A series of gas-phase experiments and extensive theoretical modeling was done on the family of singly protonated pepticles AARAA, Ac-AARAA, and AARAA-OMe. (AARAA)H+ underwent extensive H/D exchange with D2O, whereas the other two peptides with blocked termini did not, implying that a salt bridge was involved in the H/D exchange process. Ion mobility measurements and complementary molecular modeling unambiguously identified the 300 K structures of all three protonated pepticles as charge solvation structures, not salt bridges. High-level density functional theory calculations indicated the global minimum of (AARAA)H+ was a charge solvation structure with the lowest-energy salt bridge structure 4.8 kcal/mol higher in energy. Uptake of the first five water molecules of hydration at 260 K showed near identical propensities for all three pepticles consistent with a common structural motif. Quantitative measurements of DeltaHdegrees and DeltaSdegrees for the first two waters of hydration were very similar for all three pepticles, again suggestive of a common structure. A detailed search of the potential energy surface for the singly hydrated (AARAA)H+ using molecular mechanics and density functional theory approaches indicated a charge solvation structure was the global minimum, but now the lowest-energy salt bridge structure was only 1.8 kcal/mol higher in energy. Importantly, a low-energy transition state connecting the charge solvation and the salt bridge structures was found where the D2O molecule facilitated H/D exchange via the relay mechanism. This "relay" transition state was 7 kcal/mol below the (AARAA)H+ + D2O asymptotic energy, suggesting that facile H/D exchange could occur in this system. There was no equivalent low-lying relay mechanism transition state for the (Ac-AARAA)H+ and (AARAA-OMe)H+ peptides, consistent with the fact that H/D exchange was not observed. Hence, the combined experimental and theoretical methods confirmed that a salt bridge was involved in the H/D exchange by D2O of (AARAA)H+, but it existed only as a kinetic intermediate, not as a global minimum structure. These findings suggest that caution must be observed in drawing structural conclusions from H/D exchange only. A prescription is given here for understanding both the structural and H/D exchange mechanistic aspects of bare and singly hydrated peptides.